Allene oxide synthase 1 contributes to limiting grain arsenic accumulation and seedling detoxification in rice

Abstract

Arsenic (As) is a cancerogenic metalloid ubiquitously distributed in the environment, which can be easily accumulated in food crops like rice. Jasmonic acid (JA) and its derivatives play critical roles in plant growth and stress response. However, the role of endogenous JA in As accumulation and detoxification is still poorly understood. In this study, we found that JA biosynthesis enzymes Allene Oxide Synthases, OsAOS1 and OsAOS2, regulate As accumulation and As tolerance in rice. Evolutionary bioinformatic analysis indicated that AOS1 and AOS2 have evolved from streptophyte algae (e.g. the basal lineage Klebsormidium flaccidum) – sister clade of land plants. Compared to other two AOSs, OsAOS1 and OsAOS2 were highly expressed in all examined rice tissues and their transcripts were highly induced by As in root and shoot. Loss-of-function of OsAOS1 (osaos1–1) showed elevated As concentration in grains, which was likely attributed to the increased As translocation from root to shoot when the plants were subjected to arsenate [As(V)] but not arsenite [As (III)]. However, the mutation of OsAOS2 (osaos2–1) showed no such effect. Moreover, osaos1–1 and osaos2–1 increased the sensitivity of rice plants to both As(V) and As(III). Disrupted expression of genes involved in As accumulation and detoxification, such as OsPT4, OsNIP3;2, and OsOASTL-A1, was observed in both osaos1–1 and osaos2–1 mutant lines. In addition, a As(V)-induced significant decrease in Reactive Oxygen Species (ROS) production was observed in the root of osaos1–1 but not in osaos2–1. Taken together, our results indicate OsAOS1 modulates both As allocation and detoxification, which could be partially attributed to the altered gene expression profiling and ROS homeostasis in rice while OsAOS2 is important for As tolerance.

Keywords

Jasmonic acid / Arsenic tolerance / Evolutionary bioinformatics / Oryza sativa L. / ROS homeostasis

References

[1] AbbasiS, LambD, RahmanMA, et al.. Response of phosphorus sensitive plants to arsenate. Environ Technol Innov, 2021, 24: 102008 ISSN 2352-1864

[2] AntoniadisV, ShaheenSM, LevizouE, ShahidM, NiaziNK, VithanageM, et al.. A critical prospective analysis of the potential toxicity of trace element regulation limits in soils worldwide: are they protective concerning health risk assessment? - a review. Environ Int, 2019, 127: 819-847

[3] Azizur RahmanM, HasegawaH, Mahfuzur RahmanM, Nazrul IslamM, Majid MiahMA, TasmenA. Effect of arsenic on photosynthesis, growth and yield of five widely cultivated rice (Oryza sativa L.) varieties in Bangladesh. Chemosphere, 2007, 67: 1072-1079

[4] Cao Y, Sun D, Ai H, Mei H, Liu X, Sun S, Xu G, Liu Y, Chen Y, Ma LQ (2017) Knocking out OsPT4 gene decreases arsenate uptake by rice plants and inorganic arsenic accumulation in rice grains. Environ Sci Technol 51:12131–12138. https://doi.org/10.1021/acs.est.7b03028

[5] ChehabEW, PereaJV, GopalanB, ThegS, DeheshK. Oxylipin pathway in rice and Arabidopsis. J Integr Plant Biol, 2007, 49: 43-51

[6] ChenC, ChenH, ZhangY, ThomasHR, FrankMH, HeY, et al.. TBtools: an integrative toolkit developed for interactive analyses of big biological data. Mol Plant, 2020, 13: 1194-1202

[7] ChenX, JiangW, TongT, ChenG, ZengF, JangS, et al.. Molecular interaction and evolution of jasmonate signaling with transport and detoxification of heavy metals and metalloids in plants. Front Plant Sci, 2021, 12: 665842

[8] ChenY, HuaCY, ChenJX, RathinasabapathiB, CaoY, MaLQ. Expressing arsenite antiporter PvACR3;1 in rice (Oryza sativa L.) decreases inorganic arsenic content in rice grains. Environ Sci Technol, 2019, 53: 10062-10069

[9] ChenY, SunSK, TangZ, LiuG, MooreKL, MaathuisFJM, et al.. The Nodulin 26-like intrinsic membrane protein OsNIP3;2 is involved in arsenite uptake by lateral roots in rice. J Exp Bot, 2017, 68: 3007-3016

[10] ChengJ, ZhangS, YiY, QinY, ChenZH, DengF, et al.. Hydrogen peroxide reduces root cadmium uptake but facilitates root-to-shoot cadmium translocation in rice through modulating cadmium transporters. Plant Physiol Biochem, 2023, 200: 107754

[11] ClemensS, MaJF. Toxic heavy metal and metalloid accumulation in crop plants and foods. Annu Rev Plant Biol, 2016, 67: 489-512

[12] DasN, BhattacharyaS, BhattacharyyaS, MaitiMK. Expression of rice MATE family transporter OsMATE2 modulates arsenic accumulation in tobacco and rice. Plant Mol Biol, 2018, 98: 101-120

[13] DengF, LiuX, ChenY, RathinasabapathiB, RensingC, ChenJ, et al.. Aquaporins mediated arsenite transport in plants: molecular mechanisms and applications in crop improvement. Crit Rev Environ Sci Technol, 2020, 50: 1613-1639

[14] DengF, YamajiN, MaJF, LeeSK, JeonJS, MartinoiaE, et al.. Engineering rice with lower grain arsenic. Plant Biotechnol J, 2018, 16: 1691-1699

[15] DengF, YamajiN, XiaJ, MaJF. A member of the heavy metal P-type ATPase OsHMA5 is involved in xylem loading of copper in rice. Plant Physiol, 2013, 163: 1353-1362

[16] DengF, YuM, MartinoiaE, SongWY. Ideal cereals with lower arsenic and cadmium by accurately enhancing vacuolar sequestration capacity. Front Genet, 2019, 10: 322

[17] DengF, ZengF, ChenG, FengX, RiazA, WuX, et al.. Metalloid hazards: from plant molecular evolution to mitigation strategies. J Hazard Mater, 2021, 409: 124495

[18] DengF, ZengF, ShenQ, AbbasA, ChengJ, JiangW, et al.. Molecular evolution and functional modification of plant miRNAs with CRISPR. Trends Plant Sci, 2022, 27: 890-907

[19] DengM, WangS, HuangH, YeD, ZhangX, WangY, et al.. Hydrogen peroxide mediates cadmium accumulation in the root of a high cadmium-accumulating rice (Oryza sativa L.) line. J Hazard Mater, 2023, 448: 130969

[20] DuanG, KamiyaT, IshikawaS, AraoT, FujiwaraT. Expressing ScACR3 in rice enhanced arsenite efflux and reduced arsenic accumulation in rice grains. Plant Cell Physiol, 2012, 53: 154-163

[21] DuanG, ShaoG, TangZ, ChenH, WangB, TangZ, et al.. Genotypic and environmental variations in grain cadmium and arsenic concentrations among a panel of high yielding rice cultivars. Rice (N Y), 2017, 10: 9

[22] FaizanM, SeharS, RajputVD, FarazA, AfzalS, MinkinaT, SushkovaS, AdilMF, YuF, AlatarAA, AkhterF, FaisalM. Modulation of cellular redox status and antioxidant defense system after synergistic application of zinc oxide nanoparticles and salicylic acid in rice (Oryza sativa) plant under arsenic stress. Plants (Basel), 2021, 10(11):2254

[23] FarooqMA, ZhangK, IslamF, WangJ, AtharHUR, NawazA, et al.. Physiological and iTRAQ-based quantitative proteomics analysis of methyl jasmonate-induced tolerance in Brassica napus under arsenic stress. Proteomics, 2018, 18: e1700290

[24] Guan DX, Dai ZH, Sun HJ, Ma LQ (2021) Arsenic and selenium in the plant-soil-human ecosystem: CREST publications during 2018–2021. Crit Rev Environ Sci Technol 1-6. https://doi.org/10.1080/10643389.2021.2010836

[25] HaSB, LeeBC, LeeDE, KukYI, LeeAY, HanO, BackK. Molecular characterization of the gene encoding rice allene oxide synthase and its expression. Biosci Biotechnol Biochem, 2002, 66(12):2719-2722

[26] HagaK, IinoM. Phytochrome-mediated transcriptional up-regulation of ALLENE OXIDE SYNTHASE in rice seedlings. Plant Cell Physiol, 2004, 45: 119-128

[27] HayashiS, KuramataM, AbeT, TakagiH, OzawaK, IshikawaS. Phytochelatin synthase OsPCS1 plays a crucial role in reducing arsenic levels in rice grains. Plant J, 2017, 91: 840-848

[28] HuB, DengF, ChenG, ChenX, GaoW, LongL, et al.. Evolution of abscisic acid signaling for stress responses to toxic metals and metalloids. Front Plant Sci, 2020, 11: 909

[29] HuS, YuK, YanJ, ShanX, XieD. Jasmonate perception: ligand-receptor interaction, regulation, and evolution. Mol Plant, 2023, 16: 23-42

[30] HuangTL, NguyenQT, FuSF, LinCY, ChenYC, HuangHJ. Transcriptomic changes and signalling pathways induced by arsenic stress in rice roots. Plant Mol Biol, 2012, 80: 587-608

[31] Huang XY, Deng F, Yamaji N, Pinson SRM, Fujii-Kashino M, Danku J, Douglas A, Guerinot ML, Salt DE, Ma JF (2016) A heavy metal P-type ATPase OsHMA4 prevents copper accumulation in rice grain. Nat Commun 7:12138. https://doi.org/10.1038/ncomms12138

[32] HuangY, ChenH, ReinfelderJR, LiangX, SunC, LiuC, et al.. A transcriptomic (RNA-seq) analysis of genes responsive to both cadmium and arsenic stress in rice root. Sci Total Environ, 2019, 666: 445-460

[33] HungKT, HsuYT, KaoCH. Hydrogen peroxide is involved in methyl jasmonate-induced senescence of rice leaves. Physiol Plant, 2006, 127: 293-303

[34] JiangW, TongT, LiW, HuangZ, ChenG, ZengF, et al.. Molecular evolution of plant 14-3-3 proteins and function of Hv14-3-3A in stomatal regulation and drought tolerance. Plant Cell Physiol, 2023, 63: 1857-1872

[35] KamiyaT, IslamR, DuanG, UraguchiS, FujiwaraT. Phosphate deficiency signaling pathway is a target of arsenate and phosphate transporter OsPT1 is involved in as accumulation in shoots of rice. Soil Sci Plant Nutr, 2013, 59: 580-590

[36] KhannaK, KohliSK, KumarP, OhriP, BhardwajR, AlamP, et al.. Arsenic as hazardous pollutant: perspectives on engineering remediation tools. Sci Total Environ, 2022, 838: 155870

[37] Koeduka T, Ishizaki K, Mwenda CM, Hori K, Sasaki-Sekimoto Y, Ohta H, Kohchi T, Matsui K (2015) Biochemical characterization of allene oxide synthases from the liverwort Marchantia polymorpha and green microalgae Klebsormidium flaccidum provides insight into the evolutionary divergence of the plant CYP74 family. Planta 242:1175–1186. https://doi.org/10.1007/s00425-015-2355-8

[38] LeiGJ, SunL, SunY, ZhuXF, LiGX, ZhengSJ. Jasmonic acid alleviates cadmium toxicity in Arabidopsis via suppression of cadmium uptake and translocation. J Integr Plant Biol, 2020, 62: 218-227

[39] LiH, XuX, HanK, WangZ, MaW, LinY, HuaH. Isolation and functional analysis of OsAOS1 promoter for resistance to Nilaparvata lugens Stål infestation in rice. J Cell Physiol, 2022, 237(3):1833-1844

[40] LiL, ZhengQ, JiangW, XiaoN, ZengF, ChenG, et al.. Molecular regulation and evolution of cytokinin signaling in plant abiotic stresses. Plant Cell Physiol, 2023, 63: 1787-1805

[41] LiY, HuangYZ, BaoQL, HuangYC, ZhangSN. Effects of exogenous jasmonic acid on arsenic accumulation and response to stress in roots of rice seedlings. Environ Sci, 2022, 43: 4831-4838

[42] Lu X, Liu S, Zhi S, Chen J, Ye G (2020) Comparative transcriptome profile analysis of rice varieties with different tolerance to zinc deficiency. Plant Biol (Stuttg). https://doi.org/10.1111/plb.13227

[43] LuY, YeX, GuoR, HuangJ, WangW, TangJ, et al.. Genome-wide targeted mutagenesis in rice using the CRISPR/Cas9 system. Mol Plant, 2017, 10: 1242-1245

[44] MaJF, YamajiN, MitaniN, XuXY, SuYH, McGrathSP, et al.. Transporters of arsenite in rice and their role in arsenic accumulation in rice grain. Proc Natl Acad Sci U S A, 2008, 105: 9931-9935

[45] MehargAA, WilliamsPN, AdomakoE, LawgaliYY, DeaconC, VilladaA, et al.. Geographical variation in total and inorganic arsenic content of polished (white) rice. Environ Sci Technol, 2009, 43: 1612-1617

[46] MeiC, QiM, ShengG, YangY. Inducible overexpression of a rice allene oxide synthase gene increases the endogenous jasmonic acid level, PR gene expression, and host resistance to fungal infection. Mol Plant-Microbe Interact, 2006, 19: 1127-1237

[47] MousaviSR, NiknejadY, FallahH, TariDB. Methyl jasmonate alleviates arsenic toxicity in rice. Plant Cell Rep, 2020, 39: 1041-1060

[48] NazirF, FariduddinQ, KhanTA. Hydrogen peroxide as a signalling molecule in plants and its crosstalk with other plant growth regulators under heavy metal stress. Chemosphere, 2020, 252: 126486

[49] NingM, LiuSJ, DengF, HuangL, LiH, CheJ, et al.. A vacuolar transporter plays important roles in zinc and cadmium accumulation in rice grain. New Phytol, 2023, 239: 1919-1934

[50] One Thousand Plant Transcriptomes. One thousand plant transcriptomes and the phylogenomics of green plants. Nature, 2019, 574: 679-685

[51] PinsonSRM, TarpleyL, YanW, YeaterK, LahnerB, YakubovaE, et al.. Worldwide genetic diversity for mineral element concentrations in rice grain. Crop Sci, 2015, 55: 294-311

[52] PodgorskiJ, BergM. Global threat of arsenic in groundwater. Science, 2020, 368: 845-850

[53] Ronzan M, Piacentini D, Fattorini L, Federica DR, Caboni E, Eiche E, Ziegler J, Hause B, Riemann M, Betti C, Altamura MM, Falasca G (2019) Auxin-jasmonate crosstalk in Oryza sativa L. root system formation after cadmium and/or arsenic exposure. Environ Exp Bot 165:59–69. https://doi.org/10.1016/j.envexpbot.2019.05.013

[54] SeharS, AdilMF, AskriSMH, FengQ, WeiD, SahitoFS, ShamsiIH. Pan-transcriptomic profiling demarcates serendipita indica-phosphorus mediated tolerance mechanisms in rice exposed to arsenic toxicity. Rice (N Y), 2023, 16(1):28

[55] SeharS, AdilMF, MaZ, KarimMF, FaizanM, ZaidiSSA, SiddiquiMH, AlamriS, ZhouF, ShamsiIH. Phosphorus and Serendipita indica synergism augments arsenic stress tolerance in rice by regulating secondary metabolism related enzymatic activity and root metabolic patterns. Ecotoxicol Environ Saf, 2023, 256: 114866

[56] SeharS, FengQ, AdilMF, SahitoFS, IbrahimZ, BalochDM, UllahN, OuyangY, GuoY, ShamsiIH. Tandem application of endophytic fungus Serendipita indica and phosphorus synergistically recuperate arsenic induced stress in rice. Front Plant Sci, 2022, 13: 982668

[57] SharmaSS, KumarV, DietzKJ. Emerging trends in metalloid-dependent signaling in plants. Trends Plant Sci, 2021, 26: 452-471

[58] ShiS, WangT, ChenZ, TangZ, WuZ, SaltDE, et al.. OsHAC1;1 and OsHAC1;2 function as arsenate reductases and regulate arsenic accumulation. Plant Physiol, 2016, 172: 1708-1719

[59] SmirnoffN, ArnaudD. Hydrogen peroxide metabolism and functions in plants. New Phytol, 2019, 221: 1197-1214

[60] SongWY, YamakiT, YamajiN, KoD, JungKH, Fujii-KashinoM, et al.. A rice ABC transporter, OsABCC1, reduces arsenic accumulation in the grain. Proc Natl Acad Sci U S A, 2014, 111: 15699-15704

[61] SrivastavaS, SrivastavaAK, SablokG, DeshpandeTU, SuprasannaP. Transcriptomics profiling of Indian mustard (Brassica juncea) under arsenate stress identifies key candidate genes and regulatory pathways. Front Plant Sci, 2015, 6: 646

[62] Stumpe M, Bode J, Göbel C, Wichard T, Schaaf A, Frank W, Frank M, Reski R, Pohnert G, Feussner I (2006) Biosynthesis of C9-aldehydes in the moss Physcomitrella patens. Biochim Biophys Acta 1761:301–312. https://doi.org/10.1016/j.bbalip.2006.03.008

[63] SuY, McGrathS, ZhaoF. Rice is more efficient in arsenite uptake and translocation than wheat and barley. Plant Soil, 2010, 328: 27-34

[64] Sun SK, Chen Y, Che J, Konishi N, Tang Z, Miller AJ, Ma JF, Zhao FJ (2018) Decreasing arsenic accumulation in rice by overexpressing OsNIP1;1 and OsNIP3;3 through disrupting arsenite radial transport in roots. New Phytol 219:641–653. https://doi.org/10.1111/nph.15190

[65] TangZ, ChenY, MillerAJ, ZhaoFJ. The C-type ATP-binding cassette transporter OsABCC7 is involved in the root-to-shoot translocation of arsenic in rice. Plant Cell Physiol, 2019, 60: 1525-1535

[66] TangZ, ZhaoF. The roles of membrane transporters in arsenic uptake, translocation and detoxification in plants. Crit Rev Environ Sci Technol, 2021, 51: 2449-2484

[67] VermaG, SrivastavaD, NarayanS, ShirkePA, ChakrabartyD. Exogenous application of methyl jasmonate alleviates arsenic toxicity by modulating its uptake and translocation in rice (Oryza sativa L.). Ecotoxicol Environ Saf, 2020, 201: 110735

[68] Wang J, Song L, Gong X, Xu J, Li M (2020) Functions of jasmonic acid in plant regulation and response to abiotic stress. Int J Mol Sci 21. https://doi.org/10.3390/ijms21041446

[69] WangP, XuX, TangZ, ZhangW, HuangXY, ZhaoFJ. OsWRKY28 regulates phosphate and arsenate accumulation, root system architecture and fertility in rice. Front Plant Sci, 2018, 9: 1330

[70] WangP, ZhangW, MaoC, XuG, ZhaoFJ. The role of OsPT8 in arsenate uptake and varietal difference in arsenate tolerance in rice. J Exp Bot, 2016, 67: 6051-6059

[71] WasternackC, FeussnerI. The oxylipin pathways: biochemistry and function. Annu Rev Plant Biol, 2018, 69: 363-386

[72] XuJ, ShiS, WangL, TangZ, LvT, ZhuX, et al.. OsHAC4 is critical for arsenate tolerance and regulates arsenic accumulation in rice. New Phytol, 2017, 215: 1090-1101

[73] Yamaji N, Ma JF (2021) Metalloid transporters and their regulation in plants. Plant Physiol. https://doi.org/10.1093/plphys/kiab326

[74] YeM, SongY, LongJ, WangR, BaersonSR, PanZ, Zhu-SalzmanK, XieJ, CaiK, LuoS, ZengR. Priming of jasmonate-mediated antiherbivore defense responses in rice by silicon. Proc Natl Acad Sci USA, 2013, 110(38):E3631-E3639

[75] Yu LJ, Luo YF, Liao B, Xie LJ, Chen L, Xiao S, Li JT, Hu SN, Shu WS (2012) Comparative transcriptome analysis of transporters, phytohormone and lipid metabolism pathways in response to arsenic stress in rice (Oryza sativa). New Phytol 195:97–112. https://doi.org/10.1111/j.1469-8137.2012.04154.x

[76] YuX, ZhangW, ZhangY, ZhangX, LangD, ZhangX. The roles of methyl jasmonate to stress in plants. Funct Plant Biol, 2019, 46: 197-212

[77] ZhangJ, WysockiR, LiF, YuM, MartinoiaE, SongWY. Role of ubiquitination in arsenic tolerance in plants. Trends Plant Sci, 2023, 28: 880-892

[78] ZhangS, BaoQ, HuangY, HanN. Exogenous plant hormones alleviate as stress by regulating antioxidant defense system in Oryza sativa L. Environ Sci Pollut Res Int, 2023, 30: 6454-6465

[79] ZhangY, BermanA, ShaniE. Plant hormone transport and localization: signaling molecules on the move. Annu Rev Plant Biol, 2023, 74: 453-479

[80] ZhaoF, TangZ, SongJ, HuangX, WangP. Toxic metals and metalloids: uptake, transport, detoxification, phytoremediation and crop improvement for safer food. Mol Plant, 2022, 15: 27-44

[81] ZhaoFJ, AgoY, MitaniN, LiRY, SuYH, YamajiN, et al.. The role of the rice aquaporin Lsi1 in arsenite efflux from roots. New Phytol, 2010, 186: 392-399

[82] Zhou Y, Guang YL, Li JW, Wang F, Ahammed GJ, Yang YX (2019) The CYP74 gene family in watermelon: genome-wide identification and expression profiling under hormonal stress and root-knot nematode infection. Agronomy-Basel 9. https://doi.org/10.3390/agronomy9120872

[83] ZvobgoG, SagondaT, LwalabaJLW, MapodzekeJM, MuhammadN, ChenG, et al.. Transcriptomic comparison of two barley genotypes differing in arsenic tolerance exposed to arsenate and phosphate treatments. Plant Physiol Biochem, 2018, 130: 589-603